Digestion Times and Predation Potentials of Pelagia Noctiluca Eating Fish Larvae and Copepods in the NW Mediterranean Sea

Vol. 510: 201–213, 2014 MARINE ECOLOGY PROGRESS SERIES Published September 9 doi: 10.3354/meps10790 Mar Ecol Prog Ser Contribution to the Theme Section ‘Jellyfish blooms and ecological interactions’ FREEREE ACCESSCCESS Digestion times and predation potentials of Pelagia noctiluca eating fish larvae and copepods in the NW Mediterranean Sea Jennifer E. Purcell1,*, Uxue Tilves2, Verónica L. Fuentes2, Giacomo Milisenda3, Alejandro Olariaga2, Ana Sabatés2 1Western Washington University, Shannon Point Marine Center, 1900 Shannon Point Rd, Anacortes, WA 98221, USA 2Institut de Ciències del Mar, CSIC, P. Marítim 37–49, 08003 Barcelona, Spain 3Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, 73100 Lecce, Italy ABSTRACT: Predation is the principal direct cause of mortality of fish eggs and larvae (ichthyoplankton). Pelagic cnidarians and ctenophores are consumers of ichthyoplankton and zooplankton foods of fish, yet few estimates exist of predation effects in situ. Microscopic analyses of the gastric ‘gut’ contents of gelatinous predators reveal the types and amounts of prey eaten and can be used with digestion time (DT) to estimate feeding rates (prey consumed predator−1 time−1). We measured the DT and recognition time (RT) of prey for Pelagia noctiluca, an abundant jellyfish with increasing blooms in the Mediterranean Sea. DT of fish larvae averaged 2.5 to 3.0 h for P. noctiluca (4−110 mm diameter) and was significantly related to jellyfish and larval sizes. In contrast, DT of fish eggs ranged from 1.2 to 44.8 h for jellyfish ≤22 mm diameter (‘ephyrae’), but DT was not significantly related to ephyra or egg diameter. Approximately half of the eggs ingested were not digested. DT of copepods averaged 4 h. We also measured DT and RT of salps, euphausiids, and miscellaneous zooplankton. Temperature (20−25°C) generally did not significantly affect DT of any prey. Estimated potential predation effects of ephyrae on fish larvae in the Catalan Sea in 1995 showed great variability among 9 stations (0−3.7% consumed h−1). We discuss how sampling methods contributed to variation in predation estimates and offer recommendations to improve accuracy. Our results enable estimation of predation on ichthyoplankton and competition for zooplankton prey, which can have extremely important effects on fish populations globally. KEY WORDS: Anchovy · Jellyfish · Salp · Fish eggs · Ichthyoplankton · Zooplankton · Competition Resale or republication not permitted without written consent of the publisher INTRODUCTION nerability to predators (Houde 2008). ‘It is now evi- dent that high and variable predation is the principal, Much of fisheries research has been directed [proximate] agent of mortality’ (Bailey & Houde 1989, towards predicting annual recruitment of fish into Houde 2008, p 63). a fishery. The Critical Period and Aberrant Drift Many species of pelagic cnidarians and cteno- hypotheses (Hjort 1914) inspired 20th-century re - phores eat fish eggs and larvae (ichthyoplankton) cruitment fisheries oceanography research towards (reviewed by Purcell 1985, Purcell & Arai 2001), yet factors affecting the early life history of fish. The studies on the magnitude of this predation remain main factors believed to determine recruitment vari- rare. During the 1980s and 1990s, several studies ability now include the interactions of temperature quantified removal rates of ichthyoplankton by pe - and other physical processes on prey availability and lagic cnidarians and ctenophores in containers rang- larval condition, which in turn determine their vul- ing in size from 25 to 6300 l (reviewed by Purcell & *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 202 Mar Ecol Prog Ser 510: 201–213, 2014 Arai 2001). The results of those studies were affected ephyrae. We emphasized ichthyoplankton, but also by being conducted in artificial conditions (Purcell & included common zooplankton organisms. Our Arai 2001). A second approach to estimate predation objective was to measure digestion times in order to on ichthyoplankton by pelagic cnidarians and cteno- use this information in combination with gut content phores is to collect the predators in situ, thereby pre- data for P. noctiluca collected at comparable temper- serving their natural prey without experimental in- atures to calculate predator feeding rates and preda- terference. Calculation of ingestion rates (prey eaten tion effects on comparable prey. As an example, we predator−1 time−1) also requires estimation of the time used the gut content data for P. noctiluca ephyrae prey can still be recognized in gut contents; calcula- from Sabatés et al. (2010) to estimate their potential tion of predation effects (% prey standing stock con- predation on fish larvae and copepods off the Cata- sumed time−1) further requires information about the lan coast (NW Mediterranean) in 1995. abundances of the predators and prey in situ. Interest in gelatinous species has resurged re - cently, probably because of their increasing interfer- MATERIALS AND METHODS ence with human enterprises in coastal oceans (Pur- cell et al. 2007). One species of particular concern is Digestion measurements of fish larvae, fish eggs, the holoplanktonic species Pelagia noctiluca that has and zooplankton by Pelagia noctiluca medusae and caused economic damage to aquaculture in northern ephyrae were made in the Catalan Sea during Europe (Doyle et al. 2008, Raffaele 2013) and to cruises on board the RV ‘García del Cid’ (17 June to tourism, fisheries, aquaculture, and energy industries 4 July 2011 and 13 to 21 July 2012). Sea near-surface in the Mediterranean (reviewed by Mariottini et al. temperature and salinity were estimated by the 2008, Canepa et al. 2014). P. noctiluca has a long his- ship’s system. Near-ambient seawater temperature tory of blooms in the Mediterranean Sea (Goy et al. (T in °C) was maintained in the ship’s laboratory by 1989) that appear to be increasing in frequency and means of near-surface water pumped into kreisels duration (Daly Yahia et al. 2010, Kogovšek et al. and water baths containing the experimental con- 2010, Licandro et al. 2010, Bernard et al. 2011). tainers. Fish larvae, fish eggs, and zooplankton used P. noctiluca consumes a variety of prey, including for digestion measurements were selected under copepods and other crustaceans, gelatinous zoo- magnification of a dissecting microscope from plank- plankton, pelagic mollusks, appendicularians, and ton tows of a 60 cm diameter bongo net with 300 µm fish eggs and larvae (Malej 1982, Vu´cti´c 1982, mesh. Fish larvae were identified to the lowest taxon Sabatés et al. 2010, Rosa et al. 2013). Copepods were possible. Anchovy eggs were identified to species by the most numerous prey consumed by ephyrae in their oval shape. Fish larva total length (TL), copepod the NW Mediterranean Sea (Sabatés et al. 2010). cephalothorax length, and fish egg diameter were Although fish larvae averaged <1% of the available measured to the nearest 0.1 mm with calipers with mesozooplankton, they ranged from 5 to 32% of the the aid of a dissecting microscope immediately be - prey in ephyrae; anchovy Engraulis encrasicolus fore they were fed to P. noctiluca. Body lengths of larvae were the most frequently consumed (Sabatés salps (excluding protrusions) and other large species et al. 2010). Thus, P. noctiluca is potentially important were measured to the nearest 0.5 mm. Fish larval as a predator of ichthyoplankton and as a competitor length was converted to dry mass by regressions for of fish larvae and zooplanktivorous fish. Those the most similar taxa in Pepin (1995) and Rossi et al. effects are pervasive but difficult to evaluate. Be - (2006). Our methods, outlined below, were consid- cause predation effects on prey populations increase ered ‘natural feeding’ as defined by FitzGeorge-Bal- with pelagic cnidarian and ctenophore population four et al. (2013) and differed for medusae (observed sizes (Purcell & Arai 2001, Purcell & Decker 2005), visually while in kreisels) and ephyrae (observed ichthyoplankton will likely suffer greater mortality as with a dissecting microscope). populations of these predators increase. P. noctiluca medusae (>22 mm diameter) were col- The in situ feeding rates of P. noctiluca were not lected at night from the surface with a long-handled calculated from gut contents in previous studies due dip net and placed immediately in a bucket with sea- to a lack of data on the digestion times of the various water. They were kept on board in 300 l kreisels with prey types. During cruises of the FishJelly project in weakly flowing seawater, as illustrated by Purcell et 2011 and 2012, we measured digestion length of al. (2013). A prey item held with forceps and touched time and the times prey could be recognized in the to the oral arms was ingested quickly, and the inges- gastric pouches (‘guts’) of P. noctiluca medusae and tion time was recorded. After ingestion, the prey item Purcell et al.: Digestion and predation rates of Pelagia 203 was observed continuously to track its final location in dae) that had been collected during the previous the gastric pouch. Thereafter, each rapidly digesting night using a Bongo net (60 cm diameter, 300 and or transparent prey (i.e. fish larva, salp) was checked 500 µm meshes) from nearby coastal waters. These visually at ≤15 min intervals and each slowly digest- results were compared to the digestion observations ing, conspicuous prey (i.e. euphausiid) at ≤60 min made on board ship. Medusae in which the larvae intervals. Only large fish larvae, euphausiids, and could no longer be seen were also included in the salps were visible once ingested by the medusae; analysis of digestion time. therefore, fish eggs and copepods were not tested on P. noctiluca ephyrae and post-ephyrae with small medusae because they could not been seen after oral arms and tentacles (hereafter, all referred to as ingestion. The length of time that prey could still be ‘ephyrae,’ with a diameter ≤22 mm) were collected in seen in the guts was recorded and designated ‘recog- short surface hauls with a Neuston net (1.5 m2 mouth, nition time’ (RT).

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